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Inflammation and Wound Healing: the Role of the Macrophage

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Inflammation and Wound Healing: the Role of the Macrophage expert reviews http://www.expertreviews.org/ in molecular medicine Inflammation and wound healing: the role of the macrophage Timothy J. Koh1 and Luisa Ann DiPietro2,* The macrophage is a prominent inflammatory cell in wounds, but its role in healing remains incompletely understood. Macrophages have many functions in wounds, including host defence, the promotion and resolution of inflammation, the removal of apoptotic cells, and the support of cell proliferation and tissue restoration following injury. Recent studies suggest that macrophages exist in several different phenotypic states within the healing wound and that the influence of these cells on each stage of repair varies with the specific phenotype. Although the macrophage is beneficial to the repair of normally healing wounds, this pleotropic cell type may promote excessive inflammation or fibrosis under certain circumstances. Emerging evidence suggests that macrophage dysfunction is a component of the pathogenesis of nonhealing and poorly healing wounds. As a result of advances in the understanding of this multifunctional cell, the macrophage continues to be an attractive therapeutic target, both to reduce fibrosis and scarring, and to improve healing of chronic wounds. The inflammatory response following tissue injury molecular pattern molecules (DAMPs) (Ref. 1). has important roles in both normal and The hypoxic environment of the wound also pathological healing. Immediately after injury, promotes inflammation, because hypoxia the innate immune system is activated, setting in stimulates numerous cell types, including motion a local inflammatory response that macrophages, to produce mediators that are includes the recruitment of inflammatory cells important for inflammation (Ref. 2). In response from the circulation. This rapid response begins to these many signals, the levels of leukocyte with the degranulation of platelets that arrive at chemoattractants increase substantially, further the site and the injury-induced degranulation enhancing leukocyte recruitment. of resident mast cells. Local immune cells, As the recruitment of leukocytes from the including resident macrophages, are activated circulation begins in earnest, a pattern of by proinflammatory mediators released in leucocytic infiltration into the wound develops Inflammation and wound healing: the role of the macrophage response to injury, as well as damage-associated that is similar to other acute inflammatory 1 Department of Kinesiology & Nutrition, College of Applied Health Sciences, Center for Wound Healing and Tissue Regeneration, Chicago IL, USA. 2 Department of Periodontics, College of Dentistry, Center for Wound Healing and Tissue Regeneration, University of Illinois at Chicago, Chicago IL, USA. *Corresponding author: Luisa Ann DiPietro, Center for Wound Healing and Tissue Regeneration, MC 859, University of Illinois at Chicago, 801 S. Paulina, Chicago, IL 60612, USA. E-mail: [email protected] 1 Accession information: doi:10.1017/S1462399411001943; Vol. 13; e23; July 2011 © Cambridge University Press 2011 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 23 Sep 2021 at 10:40:19, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S1462399411001943 expert reviews http://www.expertreviews.org/ in molecular medicine conditions (Fig. 1). Neutrophils, the most macrophages in wound healing. Two separate abundant white cell in the circulation, infiltrate groups have used murine strains bearing the wound quickly and are the dominant macrophage-restricted expression of the human leukocyte in the earliest stages (Ref. 3). receptor for diphtheria toxin to effect a toxin- Concomitantly with the influx of neutrophils, mediated selective depletion of macrophages circulating monocytes enter the wound and before the placement of wounds (Refs 13, 14). differentiate into mature tissue macrophages The wounds of mice depleted of macrophages in (Ref. 3). Mast cell numbers in the wound also this manner exhibited delayed wound closure, increase, with most of the infiltrating mast cells decreased granulation tissue formation and originating in the adjacent tissue (Ref. 4). In the angiogenesis, decreased collagen synthesis, and late inflammatory phase of wound repair, T cells decreased levels of growth factors, including appear in the wound bed, and may influence vascular endothelial growth factor (VEGF) and the resolution and remodelling of the wound transforming growth factor-β (TGF-β). In (Refs 5, 6). As inflammation resolves and the addition, depletion of macrophages resulted in number of leukocytes diminishes, the wound reduced levels of myofibroblasts, which are undergoes a lengthy period of remodelling and contractile cell types that are important for resolution. Although inflammation is not wound closure. prominent during this resolution phase, many More recently, another group, again using a studies suggest that the events of the diphtheria toxin system, undertook a temporal inflammatory phase have profound effects on selective depletion of macrophages at sequential the final wound outcome (Refs 7, 8). Studies in times during the healing process (Ref. 15). The many different anatomical systems suggest that depletion of macrophages during the early scar formation and fibrosis may derive from inflammatory phase resulted in impaired wound inflammatory cell activity (Ref. 8). closure and granulation tissue formation. Among immune cells in the wound, the role of Depletion during the early proliferative stage the macrophage has been the subject of intensive caused severe haemorrhage and curbed later investigation, yielding more than 600 published wound closure and tissue maturation. articles on the topic within the past 5 years. The Macrophage depletion that was limited to the emerging picture demonstrates that wound tissue maturation phase had no significant effect macrophages are multifunctional and able to on healing. These studies are some of the first to influence nearly all phases of repair. Modulation delineate the different roles of macrophages of macrophage function, then, is a logical and during the phases of the healing process and rapidly emerging target for wound therapeutics. support the concept that this cell exhibits different functional phenotypes as repair Role of macrophages in wound healing progresses. Landmark studies in the early 1970s and 1980s demonstrated that macrophages are critical to Recruitment of monocytes and wound healing, and the ability of macrophages macrophages at sites of injury to produce factors that stimulate angiogenesis Similarly to leukocyte migration at almost any site and fibroplasia has been firmly established of inflammation, monocyte recruitment into (Refs 9, 10, 11, 12). Early studies used guinea wounds involves the sequential steps of pigs depleted of macrophages by treatment endothelial cell activation, cell-to-cell interaction, with both antimacrophage antiserum and and transmigration through the endothelium Inflammation and wound healing: the role of the macrophage glucocorticoids to study the role of this cell into the extravascular space. Because monocytes in the healing wound (Ref. 9). Because represent only about 3% of circulating glucocorticoids have several additional effects leukocytes, the rate of monocyte influx into that might influence repair, these early wounds is far from stoichiometric. Initially, observations were limited in interpretation. monocytes may be recruited by factors Recent advances in the use of genetically produced quickly after injury, such as split modified mice have overcome this limitation. products from the coagulation cascade, factors These techniques allow a highly selective and released from platelet degranulation and specific depletion of macrophages in wounds activated complement components. But most and have confirmed a crucial role for monocyte infiltration occurs later, and the 2 Accession information: doi:10.1017/S1462399411001943; Vol. 13; e23; July 2011 © Cambridge University Press 2011 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 23 Sep 2021 at 10:40:19, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S1462399411001943 expert reviews http://www.expertreviews.org/ in molecular medicine T cells Macrophages Neutrophils Mast cells Haemostasis Early inflammation Late inflammation Resolution/ remodelling Time after injury Pattern of leukocyte infiltration into wounds Expert Reviews in Molecular Medicine © 2011 Cambridge University Press Figure 1. Pattern of leuKocyte infiltration into wounds. Inflammatory cells are present during each of the phases of wound repair, represented here as haemostasis (yellow panel), early inflammation (light pink panel), late inflammation (dark pink panel) and resolution/remodelling (blue panel). The relative density of the four most prominent types of leuKocytes in wounds (mast cells, neutrophils, macrophages and T cells) is depicted. Whereas neutrophils and lymphocytes disappear, low numbers of resident mast cells and macrophages are present during the lengthy remodelling phase. preferential infiltration of monocytes represents (Refs 16, 17, 18, 19, 20). The role of chemokines the response to a locally produced chemotactic in the recruitment of leukocytes is complicated, gradient that specifically favours these cells. One because more than 40 chemokines have been important group of chemoattractants
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